REVIEW ARTICLEpublished: 28 May 2014

doi: 10.3389/fmicb.2014.00244

Ecological functions of zoosporic hyperparasitesFrank H. Gleason1, Osu Lilje1, Agostina V. Marano2, Télesphore Sime-Ngando3, Brooke K. Sullivan4,

Martin Kirchmair5 and Sigrid Neuhauser5,6*

1 School of Biological Sciences A12, University of Sydney, Sydney, NSW, Australia2 Núcleo de Pesquisa em Micologia, Instituto de Botânica, São Paulo, Brazil3 Laboratoire Microorganismes: Génome and Environnement, Université Blaise Pascal, Clermont-Ferrand II, Aubière, France4 Back To Nature Design, Seattle, WA, USA5 Institute of Microbiology, Leopold Franzens University Innsbruck, Innsbruck, Austria6 Microbial Diversity and Genomics, Department of Life Sciences, Natural History Museum, London, UK

Edited by:

Kevin Lafferty, US GeologicalSurvey - Santa Barbara, USA

Reviewed by:

Assaf Sukenik, Israel Oceanographicand Limnological Research, IsraelHicham El Alaoui, Université BlaisePascal - LMGE UMR CNRS 6023,France

*Correspondence:

Sigrid Neuhauser, Institute ofMicrobiology, Leopold FranzensUniversity Innsbruck,Technikerstr. 25, 6020 Innsbruck,Austriae-mail: sigrid.neuhauser@uibk.ac.at

Zoosporic parasites have received increased attention during the last years, butit is still largely unnoted that these parasites can themselves be infectedby hyperparasites. Some members of the Chytridiomycota, Blastocladiomycota,Cryptomycota, Hyphochytriomycota, Labyrinthulomycota, Oomycota, and Phytomyxea arehyperparasites of zoosporic hosts. Because of sometimes complex tripartite interactionsbetween hyperparasite, their parasite-host, and the primary host, hyperparasites can bedifficult to detect and monitor. Some of these hyperparasites use similar mechanisms astheir parasite-hosts to find and infect their target and to access food resources. The lifecycle of zoosporic hyperparasites is usually shorter than the life cycle of their hosts, sohyperparasites may accelerate the turnaround times of nutrients within the ecosystem.Hyperparasites may increase the complexity of food webs and play significant roles inregulating population sizes and population dynamics of their hosts. We suggest thathyperparasites lengthen food chains but can also play a role in conducting or suppressingdiseases of animals, plants, or algae. Hyperparasites can significantly impact ecosystemsin various ways, therefore it is important to increase our understanding about these crypticand diverse organisms.

Keywords: hyperparasites, ecology, food web, parasite, zoospores, eDNA

INTRODUCTION

“So, naturalists observe, a fleaHas smaller fleas that on him prey;And these have smaller still to bite ‘em,And so proceed ad infinitum.”Jonathan Swift, On Poetry: a rhapsody (1733)

Parasites belonging to all taxonomic groups have gainedincreasing attention in ecological research during recent years.It is widely recognised that the number of species of parasitesare more numerous than organisms with a non-parasitic lifestyle(Lafferty et al., 2008). Also it is widely accepted that many par-asites can themselves be hosts for other parasites. Such parasitesof parasites are usually called “hyperparasites”; a term which isused without any reference to the phylogeny of the host or theparasite or whether the relationship is obligately or facultativelyparasitic. Novel methodological tools and an increasing interestin parasites and their ecology have led to more targeted samplingapproaches. This has shown that especially microbial parasiteswhich have until now been rarely detected are abundant anddiverse (Lefèvre et al., 2008; Jones et al., 2011; Hartikainen et al.,2014). It is very difficult—or in many cases impossible—to iso-late and identify them because of their generic morphology, andbecause such parasites are often restricted to only a few host cellswhich makes them difficult to detect even with state of the art

molecular methods. Hence, it is no surprise that microbial hyper-parasites are not well understood. Some species of hyperparasitesare endoparasites and difficult to see in the light microscope with-out special staining methods. Although zoosporic parasites ofprimary producers have been the focus of recent studies (Powell,1993; Ibelings et al., 2004; Kagami et al., 2007; Marano et al.,2011; Neuhauser et al., 2011a), our knowledge about zoosporichyperparasites and their microbial hosts remains anecdotal. Inthis article we focus on zoosporic hyperparasites with zoosporichosts, their abundance and relationships between parasites andtheir hosts and their possible roles in ecological processes.

In two of the early works focusing on microbial hyper-parasites, Karling (1942a,b) documented and discussed exam-ples of hyperparasitism among zoosporic true fungi (Table 1).Although his study focused primarily on hyperparasites amongthe zoosporic true fungi, Karling was aware of hyperparasitesamong other microbial groups such as stramenopiles or plas-modiophorids (Table 2). Sparrow’s monograph about aquaticphycomycetes contains still the most comprehensive referencesto zoosporic hyperparasites (Sparrow, 1960). Although hyper-parasitism among true fungi has been the focus of numer-ous research projects, for instance in the form of biologicalcontrol of plant diseases (e.g., Vinale et al., 2008), hyperpara-sitism involving heterotrophic stramenopiles and zoosporic truefungi has been rare (Boosalis, 1964; Barnett and Binder, 1973;Adams, 1990). Zoosporic hyperparasites have been described

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Table 1 | Selected hyperparasitic Opistokonts (Chytridiomycota, Cryptomycota, Blastocladiomycota).

Hyperparasite Trophic Parasite Host (=Host of parasite) References

mode (=Host of hyperparasite)

Cryptomycota Chytridiomycota

Rozella marina Biotroph Chytridium polysiphoniae Parasite, red algae Sparrow, 1960; Held, 1981

Rozella parva Biotroph Zygorhizidium affluens Canter, 1965; Beakes et al., 1988

Rozella rhizophlyctii Biotroph Rhizophlyctis rosea Facultative parasite Karling, 1960; Held, 1981

Biotroph Rhizophydium globosum Parasite, Diatoms, algae Sparrow, 1960; Held, 1981

Rozella polyphagi Biotroph Polyphagus laevis Parasite, Euglena Sparrow, 1960; Held, 1981

Biotroph Polyphagus euglenae Parasite, Euglena Powell, 1984

Rozella endochytrium Biotroph Endochytrium operculatum Facultative parasite, algae Sparrow, 1960; Held, 1981

Rozella cladochytrii Biotroph Cladochytrium replicatum Facultative parasite, green algae Sparrow, 1960; Held, 1981

Cryptomycota Blastocladiomycota

Rozella allomycis Biotroph Allomyces arbuscula Facultative parasite, insect cadaver Held, 1981

Biotroph Allomyces macrogynus Held, 1974

Cryptomycota Oomycota

Rozella rhipidii-spinosi Biotroph Araiospora spinosa Facultative parasite Sparrow, 1960; Held, 1981

Rozella apodiae-brachynematis Biotroph Apodachlya brachynema Facultative parasite Sparrow, 1960; Held, 1981

Rozella achlyae Biotroph Achlya flagellata Facultative parasite Sparrow, 1960; Held, 1981

Dictyuchus anomalus Parasite, fish

Rozella cuculus Biotroph Pythium intermedium Parasite, plant Sparrow, 1960; Held, 1981

P. monospermum Parasite, nematode Held, 1981

Rozella laevis Biotroph Pythium gracile Parasite, green algae Sparrow, 1960; Held, 1981

Rozella barrettii Biotroph Phytophthora cactorum Parasite, plant Sparrow, 1960; Held, 1981

Rozella pseudomorpha Biotroph Lagenidium rabenhorstii Parasite, green algae Sparrow, 1960; Held, 1981

Chytridiomycota Chytridiomycota

Dictyomorpha dioica Biotroph Achlya flagellata Mullins and Barksdale, 1965

Chytridium parasiticum Biotroph Septosperma rhizophydii Parasite, chytrid Karling, 1960

Rhizophydium parasiticum Rhizophlyctis rosea Facultative parasite, chitin Karling, 1960; Sparrow, 1960

Chytridiomyces verrucocsa

Rhizophydium carpophilum Synchytrium fulgens Parasite, plant Karling, 1960

S. macrosporum Parasite, plant

S. linariae Parasite, plant

Phlyctochytrium synchytrii Synchytrium endobioticum Parasite, plant Karling, 1942a

Septosperma rhizophydii Rhizophydium macrosporum Facultative parasite Karling, 1960

Septosperma anomala Phlyctidium bumelleriae Parasite, Xanthophyceae Karling, 1960

Chytridiomycota Oomycota

Rhizophydium pythii Biotroph Pythium monospermum Parasite, nematode Sparrow, 1960

Rhizidiomyces japonicus Phytophthora megasperma Parasite, plant Sneh et al., 1977

Phytophthora erythroseptica Parasite, plant Wynn and Epton, 1979

Canteriomyces stigeoclonii Phytophthora megasperma Parasite, plant Sneh et al., 1977

Blastocladiomycota Oomycota

Catenaria anguillulae Facultative Phytophthora cinnamomii Parasite, plant Daft and Tsao, 1984

Phytophthora parasitica Parasite, plant

Hyperparasites and hosts are sorted by taxon. Higher ranks are given in bold.

in the fungal groups Chytridiomycota, Blastocladiomycota, andCryptomycota (Opisthokonts, for examples see Table 1). Withinthe heterokonts the groups Hyphochytriomycota, Oomycota,Labyrinthulomycota, and Phytomyxea contain hyperparasiticspecies (Table 2). These groups belong to various supergroupsin the tree of life (Baldauf, 2003; Adl et al., 2012), but

these microorganisms interact together in the same ecosystems.Because of their morphological similarity and their similarityin size they can have ecologically similar functions and are infood web studies often treated as “trophic species” (Powell, 1993;Marano et al., 2011). Many of the known hosts belong to com-mon genera which are frequently observed in many soil and fresh

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Table 2 | Selected hyperparasitic Heterokonts (Oomycota, Hyphochytridiomycota, Phytomyxea).

Hyperparasite Trophic Parasite Host (=Host of parasite) References

mode (=Host of hyperparasite)

Oomycota Oomycota

Olpidiopsis incrassata Saprolegnia ferax Parasite, fish Slifkin, 1961

Olpidiopsis karlingiae Rhizophlyctis rosea Facultative Parasite Karling, 1960

Pythiella vernalis Pythium aphanidermatum Parasite, plant Pires-Zottarelli et al., 2009

Pythium gracile Parasite, green algae Blackwell, 2010

Pythiella pythii Pythium dictyosporum Parasite, green algae Blackwell, 2010

Pythium proliferum Rhizophlyctis rosea Facultative Parasite Karling, 1960

Pythium monospermum Phytophthora megasperma Parasite, plant Humble and Lockwood, 1981

Pythium oligandrum Pythium irregulare Parasite, plant Ribeiro and Butler, 1995;Benhamou et al., 1999

Pythium mamillatum Parasite, plant

Pythium paroecandrum Parasite, plant

Pythium aphanidermatum Parasite, plant

Pythium sylvaticum Parasite, plant

Pythium ultimum Parasite, plant

Hyphochytridiomycota Oomycota

Hyphochytrium catenoides Facultative Pythium myriostylum Parasite, plant Ayers and Lumsden, 1977

Aphanomyces euteiches Parasite, plant Ayers and Lumsden, 1977; Snehet al., 1977

Phytophthora erythroseptica Parasite, plant Wynn and Epton, 1979

Phytophthora megasperma Parasite, plant Humble and Lockwood, 1981

Phytomyxea Oomycota

Sorodiscus cokeri Biotroph Pythium proliferum Facultative Parasite Goldie-Smith, 1951

Pythium graminicolum Facultative Parasite, moss Goldie-Smith, 1951

Pythium catenulatum Facultative Parasite, plant Goldie-Smith, 1951

Pythium elongatum Facultative Parasite Goldie-Smith, 1951

Pythium irregulare Parasite, plant Goldie-Smith, 1951

Pythium undulatum Parasite, plant Goldie-Smith, 1951

Woronina polycystis Biotroph Saprolegnia ferax Parasite, fish Goldie-Smith, 1954

Woronina pythii Biotroph Pythium proliferum Facultative Parasite Goldie-Smith, 1956a

Pythium aphanidermatum Parasite, plant Goldie-Smith, 1956a

Pythium debaryanum Parasite, plant Goldie-Smith, 1956a

Pythium irregulare Parasite, plant Goldie-Smith, 1956a

Pythium monospermum Parasite, nematode Goldie-Smith, 1956a

Pythium pulchrum Goldie-Smith, 1956a

Pythium ultimum Parasite, plant Goldie-Smith, 1956a

Hyperparasites and hosts are sorted by taxon. Higher ranks are given in bold.

water ecosystems using both baiting procedures and molecularanalysis of environmental samples (Sparrow, 1960; Powell, 1993;Barr, 2001; Dick, 2001; Lozupone and Klein, 2002; Shearer et al.,2007; Lefèvre et al., 2008; Marano et al., 2011). It is very likelythat zoosporic hyperparasites are as abundant on “rarer” hosts.This is of ecological importance because zoosporic true fungiand heterotrophic stramenopiles can be among the predomi-nant groups in some ecosystems (Lefèvre et al., 2008; Freemanet al., 2009; Marano et al., 2011). Because of the large numberof species of zoosporic parasites, hyperparasites, and their asso-ciated hosts, it is likely that there are many additional taxa thatawait discovery.

ZOOSPORESZoospores are a shared morphological feature of the hosts andhyperparasites discussed here. Zoospores are motile propaguleswhich permit rapid dispersal. Zoospores can sense environmen-tal gradients which they use to identify and find potential hosts(Tyler, 2002). There are different types of zoospores (Langeand Olson, 1983), which have distinguishing features, allowingobservers to determine and categorize the organisms. The mostimportant feature is the type of flagellation. Zoospores can gen-erally be grouped into (1) uniflagellate with posteriorly directedwhiplash flagellum, (2) uniflagellate with an anteriorly directedtinsel flagellum, (3) biflagellate, heterokont, with one posteriorly

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directed whiplash flagellum and one anteriorly directed tinselflagellum and (4) biflagellate, isokont, two whiplash flagellae,often of different lengths, with the shorter one anteriorly directedand the longer one posteriorly directed.

Despite their relatively simple morphology many zoosporichyperparasites form functionally and developmentally distincttypes of zoospores during their life cycle (Sparrow, 1960). A vari-ety of names are used for different types of zoospores in differenttaxonomic groups, but generally one type of zoospore is formedin zoosporangia following mitosis and can be either haploid ordiploid, while another type of zoospore is formed by meiosisand is haploid (Lange and Olson, 1983). The different types ofzoospores can serve different functions during the parasite lifecycle—such as rapid propagation and dispersal or primary infec-tion and population establishment after periods of hibernation(e.g., Neuhauser et al., 2011b). Despite variable modes of forma-tion and complex parasite life cycles which can result in periodswhere one type of zoospore is predominantly formed, the mainunifying feature of all types of zoospores is that they are small,single-celled, motile propagules. Within food webs zoosporesprovide a rapid energy source for a variety of organisms at highertrophic levels (Gleason et al., 2011), so it is not surprising thatzoospores are often treated as trophic species.

MECHANISMS USED BY HYPERPARASITES TO ACCESSFOOD RESOURCESZoosporic hyperparasites use a large variety of mechanismsto attack their hosts. Hyperparasites can grow epibioticallyon the surface of their host only entering the host cell withspecialized structures such as chytrid rhizoids (Figures 1A,C).Hyperparasites also grow endobiotically this means completelysubmerged in their hosts (Figures 1B,D). The parasite hosts ofhyperparasites can be ectoparasites (Figures 1A,B) growing epibi-otically on the primary host or endoparasites (Figures 1C,D)growing endobiotically inside the primary host. Hyperparasiteswhich are infecting ectoparasites only have to overcome thedefense mechanisms of their host, and often use infection strate-gies that are very similar to those of zoosporic parasites (Sparrow,1960; Marano et al., 2012). On the other hand, hyperparasiteswhich are parasites of endoparasites may have to overcome twobarriers of defense—they have to enter the parasite-host andtheir host to get access to food resources. Most of the describedzoosporic hyperparasites are parasites of ectoparasites (e.g., mostRozella species, Wornina spp.). We hypothesize that ectopara-sites are easier accessible for hyperparasites with only one line ofdefense to break. We also hypothesize that our knowledge aboutzoosporic hyperparasites of endoparasites is biased by the factthat zoosporic endoparasites are a poorly studied group them-selves. Therefore, most of the examples discussed here are fromzoosporic hyperparasites of parasites which are not completelysubmerged inside their host or from endoparasitic hyperparasitesof epibiotic hosts (Figures 1A–C).

An example of an epibiotic infection (Figure 1A) is the par-asitic relationship between the two chytrids Chytriomyces verru-cosus and Rhizophlyctis rosea (Karling, 1960). The chemotacticzoospores of R. rosea are attracted to the host cell where theyencyst. The zoospore then germinates and a germ tube penetrates

FIGURE 1 | Types of hyperparasitism. Blue—primary host,green—parasite, red—hyperparasite. (A) epibiotic hyperparasite ofectoparasite. This type can be found for example in the interaction of thehyperparasite Rhizophydium parasiticum (Chytridiomycota), its and its(facultative) parasites host Rhizophlyctis rosea. (B) Endobiotic hyperparasiteof ectoparasite host. This is the most commonly described mode ofhyperparasitsm seen in many Rozella species (Cryptomycota) or Woroninaspp. (Phytomyxea). (C) Epibiotic hyperparasite of endoparasite host. E.g.,Rhizophyidum carpophilum (Chytridiomycota) on Olpidiopsis sp.(oomycetes) and Synchytrium sp. (chytrid). (D) Endobiotic hyperparasite ofendoparasite host. E.g., the hyperparasitic chytrid Phlyctochytriumsynchytrii in the plant pathogen Synchytrium endobioticum.

the host zoosporangium. Inside the host, an endobiotic rhizoidalsystem develops supplying the epibiotic zoosporangium (havingsince formed from the body of the zoospore) with nutrients.Epibiotic parasites can also be found in the stramenopiles (Snehet al., 1977): zoospores of the hyphochytriomycete Rhizidomycesjaponicus attach to the surface of oospores of Phytophthoramegasperma (Oomycetes) where thalli grow externally aroundthe oospore and produce zoosporangia. The oomycete Pontismalagenidioides which is a parasite of the green alga Chaetomorphamedia can be infected by Labyrinthula sp. (Raghukumar, 1987).

Endobiotic parasites grow entirely submerged within theirhost. An example is Rozella allomycis (Rozellida/Cryptomycota)and its host Allomyces arbuscula (Blastocladiomycota) (Held,1973, 1974). In this case, the infection process is relatively wellstudied and is described in more detail here to exemplify theinfection process of most known endobiotic zoosporic hyperpar-asites. Substances produced by the host attract the chemotacticzoospores of the parasite toward the host. Once the zoosporeattaches to the surface of the host cell it forms a so-called cyst,which produces a germ tube. The germ tube then grows intothe host cell through the cell wall while the protoplast of Rozellais pushed into the host cell by fluid pressure produced from avacuole in the cyst. Subsequently the parasite grows inside thehost cell. In the case of Rozella allomycis the host cell is thentransformed into the parasite sporangium. Other known endo-biotic parasites are Rozella polyphagi (Rozellida/Cryptomycota),which parasitizes the chytrid parasite Polyphagus euglenae

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(Powell, 1984) and the endobiotic parasite Catenaria allomycis(Blastocladiomycota), which infects Allomyces javanicus (Sykesand Porter, 1980; Powell, 1982). Catenaria anguillulae, a mem-ber of the Blastocladiomycota, is an endobiotic parasite of theplant pathogenic oomycetes Phytophthora cinnamomi and P. par-asitica (Daft and Tsao, 1984), while Hyphochytrium catenoides(Hyphochytriomycota) colonizes oospores of Pythium myriosty-lum (Ayers and Lumsden, 1977). Another parasite of Pythiumspp. is Woronina pythii (Phytomyxea), which infects both vege-tative hyphae and reproductive structures of Pythium (Dylewskiand Miller, 1983).

Interactions are slightly different between hyphal formingzoosporic organisms, such as oomycetes. Here interactionsbetween hyphae can be observed, and these interactions aredifferent from the endo- and epibiotic parasitic interactions dis-cussed above. Two distinct mechanisms appear to be involvedin interactions between this parasite and its hosts: (1) hyper-parasitism; mediated by hyphal interactions, and (2) antibiosis;causing metabolic and developmental changes prior to con-tact between hyphae of the parasite and host (Adams, 1990;Benhamou et al., 1999). An example of direct interactionsbetween the organisms is the interaction between hyphae of thewell-known hyperparasite Pythium oligandrum (Oomycota) andhyphae of its oomycete hosts (e.g., P. ultimum, P. aphaniderma-tum, Phytophthora megasperma) (Benhamou et al., 1999). Hyphaeof the parasite can adhere to the surface of the host sometimescoiling around the host hyphae. Penetration of the host cells byinfection pegs may follow, leading to digestion of the host cyto-plasm. When the interaction is initiated by antibiosis (withoutcontact with the host) the parasite can release soluble substanceswhich cause biochemical changes within the host cells. Then theparasite can release extracellular enzymes, which digest the hostcells.

BIODIVERSITY AND HOST RANGE OF HYPERPARASITESDNA sequences assigned to putative parasite and hyperpara-site taxa of zoosporic fungi are widespread (e.g., Lara et al.,2010; Jones et al., 2011; Lara and Belbahri, 2011; Nagano andNagahama, 2012). But molecular methods are often biased bythe selection of primers and sampling methods (Hartikainenet al., 2014; Neuhauser et al., 2014) and the assignment of envi-ronmental DNA sequences to described species is only as goodas the available reference datasets. Data on zoosporic microor-ganisms are sparse, and many of the “unknown” sequences areprobably from common species which to date have no refer-ence record in public data bases (e.g., Nagy et al., 2011; Karpovet al., 2013). Reliable reference sequences of many zoosporichyperparasites are generally rare. One reason is that many of theknown zoosporic hyperparasites are biotrophic parasites whichcannot be grown without their hosts. The hosts themselves areoften biotrophic parasites as well, making it very hard to iso-late, identify and sequence the hyperparasites. Therefore, tar-geted studies to detect and characterize hyperparasites and theirhosts are needed. Such targeted approaches could include bait-ing experiments combined with microscopic observation or DNAand RNA based screenings of various environments. Despitebeing very time consuming baiting and isolation experiments

are highly valuable because they will allow to understand howhyperparasites interact with their hosts, to describe their lifecycle, and to analyze interactions with their hosts. Baiting exper-iments with oospores of the oomycetes parasites Phytophthoramegasperma, P. cactorum, Pythium sp. and Aphanomyces euteiches,revealed that those baits quickly became infected by differenthyperparasites (Sneh et al., 1977). Another approach for char-acterizing zoosporic hyperparasites would be to implement acombination of DNA and RNA isolation methods combined withspecific primers and to then visualize the respective organismsusing specific FISH (Fluorescence in situ hybridization) probes(Not et al., 2002; Jones et al., 2011; Marano et al., 2012). Suchtargeted molecular probing techniques are a powerful tool toidentify unknown organisms. When attempting to detect hyper-parasites by this approach, however, mainly free living stages(zoospores) will be detected and the sampling is largely limitedto aquatic environments because the background fluorescence insoil or sediment samples tends to be high (Wagner and Haider,2012).

Hyperparasites, their hosts and the primary hosts are com-plex systems. Most studies about zoosporic hyperparasites basetheir evidence on laboratory studies of dual cultures of one hostinfected by one parasite or the host range of a single parasite(e.g., Karling, 1960; Sparrow, 1960; Held, 1981). Although todate we can only estimate how those interactions might occurin natural environments like sediment or soil (Gleason et al.,2012), simultaneous infections by different species are likely—especially for abundant parasite hosts for which more than onespecies of hyperparasite is known (for examples see Tables 1, 2).Similarly, unrelated or distantly related hyperparasites may infectthe same hosts individually or simultaneously. An excellent exam-ple of this phenomenon was described by Karling (1960) whoobserved simultaneous infection of Rhizophlyctis rosea with fourhyperparasites. He studied infections of the facultative parasiteR. rosea with Chytriomyces verrucosa (Chytridiomycota). Karlingnoted that numerous sporangia of R. rosea were also infected withRozella rhizophlyctii (Rozellida/Cryptomycota) and Olpidiopsiskarlingiae (Oomycota). In addition to this, the large sporangiaof R. rosea were infected by a fourth species, Pythium proliferum(Oomycota), which was itself densely parasitized by Woroninapythii (Phytomyxea). Although R. rosea is a facultative parasite,this example shows the extent to which hyperparasites can occurin nature when studied in detail.

On the other hand not all hyperparasites are host specific.Studies on the range of host specificity indicate that somespecies of hyperparasites in the Oomycota and Phytomyxea caninfect several species of hosts (Goldie-Smith, 1951; Dylewskiand Miller, 1983). Rozella allomycis only infects two suscepti-ble hosts: Allomyces arbuscula and A. macrogynus (Held, 1974),while Olpidiopsis incrassata infects six species of Saprolegnia andthree species of Isoachlya (Slifkin, 1961). Other parasites suchas Woronina pythii have a broad host spectrum and can infectmore than 40 species of oomycetes (Dylewski and Miller, 1983).Pythium oligandrum also infects a wide range of fungal andstramenopilous host (Ribeiro and Butler, 1995). These studieshighlight the importance of isolating and characterizing speciesfor understanding and characterizing hyperparsite biodiversity

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and host range. Culture based methods and well defined voucherisolates are also needed to provide a groundwork for DNA bar-coding studies (del Campo et al., 2014) or for food web analyses(Hrcek et al., 2011) which form the basis for a more holisticunderstanding of hyperparasites and their ecological roles.

SIZE CONTROL OF HOST POPULATIONS BYHYPERPARASITESLike all parasites, hyperparasites can impact population size andfitness of their hosts (Sieber and Hilker, 2011; Allen and Bokil,2012; Preston et al., 2014). Some hyperparasites can infect per-sistent structures of their hosts, for example oospores, resistantsporangia, or resting spores (Gleason et al., 2010). Such restingstages are recalcitrant substrates and can survive in a dormantstate in dried soil for long periods of time (Goldie-Smith, 1956b;Bruckart et al., 2011) where they accumulate, forming a “sporebank” of zoosporic parasites. But when these resting stages areinfected by hyperparasites the pathogen pressure can potentiallybe reduced. This could explain the finding that zoosporic hyper-parasites can be linked to suppressive soil properties (Weller et al.,2002) as they have the ability to reduce the viable pathogen loadin soil. The presence of hyperparasites contributes to control-ling their hosts in the environment, hinting at the important roleof these parasites in balancing diversity and abundance of theirhosts, consequently resulting in stable ecosystems.

Hyperparasites are already widely used as biological controlagents to control the population size of plant pathogens. The bestknown example is the oomycete Pythium oligandrum which isused to control other Pythium spp. and oomycetes (Ikeda et al.,2012). Hyperparasites have a huge potential to control diseasesif they can be systematically accumulated in the environment.But so far not many hyperparasites can be grown in the lab inbig enough quantities that permit use as biocontrol agent. Thereare known hyperparasites of important plant pathogens whichhave not been explored as biocontrol agents because of this rea-son. Oospores of the potato pathogen Phytophthora erythrosep-tica, for example, were found to be infected with Hyphochytriuncatenoides and Rhizidiomyces japonicus in waterlogged soils inEngland (Wynn and Epton, 1979). Given the global importanceof Phytophthora spp. as existing and emerging plant pathogens(Brasier et al., 2004; Fry, 2008; Fisher et al., 2012), identifyinghyperparasites that naturally control the abundance and survivalof these parasites would be beneficial.

There have been observations of such effects in control ofpopulation sizes by hyperparasites in fresh water ecosystems.Populations of Zygorhizidium affluens (Chytridiomycota) are fre-quent parasites of populations of the diatom Asterionella formosain freshwater lakes (Canter, 1965; Beakes et al., 1988). The growthof the parasite population follows the growth of the host popu-lation (Chave, 2013) resulting in a “chytrid epidemic.” Sporangiaand resting spores of Z. affluens can be infected by the hyperpara-site Rozella parva (Canter, 1965). Both a decline in the A. formosapopulations and an increase in the R. parva populations as thegrowing season progresses would, in theory, result in a decrease inZ. affluens populations. Another example is Polyphagus euglenae,a parasite of Euglena viridis and E. gracilis and its hyperparasiteRozella polyphagi (Powell, 1984), in which an infection with the

hyperparasite R. polyphagi is known to decrease the populationsize of its host. Blooms of toxic cyanobacteria are common infreshwater environments (Sønstebø and Rohrlack, 2011). Thesecyanobacteria can be parasitized by zoosporic true fungi (Canter,1972) that have the potential to control the sizes of such toxicalgal blooms. Parasites of cyanobacteria can be infected by hyper-parasites, a fact which was noted, but not analyzed in any detail.A reduction in the numbers of zoosporic parasites may result inan increase in growth of the (toxic) algal blooms (Canter, 1972).However, such tripartite interactions should be the subject offuture studies: hyperparasites may impact the population sizesof parasitic, zoosporic true fungi that are parasites of organismswhich can be damaging to the environment. The need to study theecological role of hyperparasites may be even more significant ascyanobacteria and microalgae are gaining increasing importanceas sustainable second generation biofuels (Stephens et al., 2010).Microalgal cultures are prone to get contaminated with a widerange of bacteria and eukaryotes which potentially impact on theyield (Stephens et al., 2010; Lakaniemi et al., 2012). Especially insuch semi-controlled systems a control of detrimental parasiteswith hyperparasites could be a successful approach to increaseproductivity and energy yield.

FOOD WEBSThe presence of hyperparasites in food webs affect predators andgrazers alike (Figure 2) (Hatcher et al., 2006; Morozova et al.,2007). By infecting resistant structures of their hosts, zoosporicparasites and hyperparasites release recalcitrant carbon, whichis then potentially made available as food for protistan andmetazoan predators rather than being deposited through sedi-mentation (Figure 2D). When zoospores are released, some willfind new utilizable substrates, some will encyst, but many mayprovide food for grazing zooplankton and filter feeding ani-mals (Figure 2A) (Kagami et al., 2007; Miki et al., 2011). Thesizes of the mouth parts of grazing zooplankters determines themaximum size of zoopores that can be ingested (Kagami et al.,2007). For example, species of Daphnia are known to digestzoospores of any species smaller than 5 µm in diameter. The sizesof zoospores of hyperparasites tend to be smaller than those ofthe hosts (Sparrow, 1960; Held, 1981). This is clearly exempli-fied by the parasitic relationship between the fish parasite Achlyaflagellata and its hyperparasite Dictyomorpha dioica (Mullins andBarksdale, 1965). The zoospores of A. flagellata are 8.5–10.5 µmin diameter while those of D. dioica are 3.5 µm in diameter(Mullins and Barksdale, 1965). The smaller size of the hyper-parasite zoospores may enable zooplankton to graze on them ormake their ingestion by zooplankters more likely, so that theyultimately provide better food resources for zooplankton thanparasite zoospores. The population sizes of key species of grazingzooplankters, such as Daphnia, may be impacted by a decrease orincrease in the total supply of zoospores which are a good foodsource (Kagami et al., 2007). This in turn will impact the popu-lation sizes of planktonivorous fish and other macroinvertebrateswhich feed on zooplankton.

Because of the high nutritional value of zoospores, we wouldexpect populations of Daphnia magna to increase with the onsetof the chytrid epidemic. Daphnia magna also feeds on zoospores

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FIGURE 2 | Possible links of a hypothesized food web in which

zoosporic parasites and hyperparasites are involved. In food webszoosporic hyperparasites can either contribute the zoospore pool (Zoosporepool, A) which is used as food source by grazers in terrestrial and acquaticecosystems. At the same time epibiotic sporangia of hyperparasites(Epibiotic, B) can serve as food source for larger grazers. The sporangia ofepibiotic hyperparasites (Endobiotic, C) are more difficult to access as food

sources for grazers. Some zoosporic hyperparasites use resting stages(Reservoirs, D) as substrate. Hosts of hyperparasites can be parasites ofmicroscopic eukaryotes, but also parasites of plants or animals. This allowsfor a rapid cycling of nutrients from organisms higher up in the food webtowards small grazers (trophic upgrading). References: zoos, zoosporangium;host, zoosporic host; oos, oospore; rsp, resting spore; rspr, restingsporangium.

of Batrachochytrium dendrobatidis (Chytridiomycota), which is aserious pathogen of amphibians (Buck et al., 2011). It was sug-gested that the consumption of zoospores of B. dendrobatidis byD. magna may prevent the transmission of this fungus (Buck et al.,2011). If a crash occurs in populations of D. magna, when thetotal zoospore food supply rapidly decreases, the rate of transmis-sion of amphibian chytridiomycosis could increase because fewerindividuals of D. magna would be present to feed on zoosporesof B. dendrobatidis. Thus, more zoospores would be available tospread chytridiomycosis through the populations of amphibians.In adult frogs B. dendrobatidis prevalence is highest during latesummer and winter, while infection takes place from late springto early summer (Russell et al., 2010; Sapsford et al., 2013). Thiscoincides with the breakdown of the chytrid epidemics. We wouldexpect many other biotic and abiotic factors to affect populationdynamics here, but the availability of zoospores as food in thespring can be decisive for the pathogen load of B. dendrobatidislater in the year by influencing the numbers of predators feedingon zoospores.

It is important to establish the roles of zoosporic hyperpara-sites as well as parasites in the structure and function of aquaticfood webs. Structure includes species richness, trophic levels,links, trophic chain length, and connectance (Dunne et al., 2005,2013). Function includes the total amount, rate, and efficiency ofcarbon transfer, and effects on stability of the food web. Addingparasites to food webs results in an increased complexity (Laffertyet al., 2008; Thieltges et al., 2013). Adding links to food webs, suchas parasites, hyperparasites, and both of their associated niches,

might also add to the stability of a particular web (Hudson et al.,2006; Lafferty et al., 2006, 2008). Parasites with life cycles involv-ing ontogenetic niche shifts—such as hyperparasites—impactfood web structures more and potentially negatively because spe-cialized life cycle stages are more prone to secondary extinctionthan generalist stages (Preston et al., 2014). Such ontogeneticeffects can be found in zoosporic hyperparasites: different types ofzoospores, or zoospores formed by different species can have con-siderably different swimming patterns (Lange and Olson, 1983)or serve different purposes like long or short distance dispersal(Neuhauser et al., 2011a). Consequently different zoospores willattract predators occupying different niches and will thereforeenter the food web at different trophic levels. Because of the anec-dotal nature of the available data it is not yet possible to includezoosporic hyperparasites into mathematical food web models toallow for more realistic estimates of population dynamics andenergy flow and their impact on food web stability. However, itcan be expected that once our knowledge about zoosporic hyper-parasites increases, we will also be able to show that, like zoosporictrue fungi, zoosporic hyperparasites are diverse, abundant, andimportant links for energy transfer (Grami et al., 2011; Niquilet al., 2011). Zoosporic true fungal parasites result in a signifi-cant reduction in the loss of algal carbon though sedimentationinto the detritus pool, allowing carbon transfer from zoosporesto grazing protists and metazoans. This contributes to longer car-bon path lengths, higher levels of activity and specialization, lowerrecycling, and increased stability of aquatic food webs (Gramiet al., 2011; Ulanowicz et al., 2014).

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Hyperparasites tend to have shorter life cycles than their hosts,so they produce biomass in the form of zoospores more quickly.Some of them produce primarily zoospores, such as Rozella,which, instead of forming its own zoosporangium, uses the hostsporangium to reproduce (Held, 1981; Powell, 1984). This out-sourcing of energy consuming biomass production allows forfaster life cycles and hyperparasites such as Rozella are there-fore likely to increase and accelerate the energy flow betweentrophic levels (Figure 2C). On the other hand epibiotic para-sites have zoosporangia that are formed on the surface of theirhost. Consequently, both their zoospores and the zoosporan-gia are likely to enter the food web contributing different typesof energy for predators with different size preferences for theirfood (Figure 2B). Since food webs that include zoosporic hyper-parasites have additional links, we suggest they could be moreefficient, and therefore would support a larger population ofgrazing zooplankton species. This hypotheses needs to be testedquantitatively.

CONCLUSION AND FUTURE PROSPECTSMany hyperparasites have been discovered during researchwith the host species. However, it is vital that such efforts areintensified to provide the basis for the development of morerapid tools for species discovery and characterization. Althoughemerging techniques such as single cell genomic approachesprovide a quantum leap in identifying and characterizing activecells in the environment, such methods will initially not accountfor the complex life cycles of zoosporic hyperparasites. To under-stand the life cycles, and consequently the ecological functionof hyperparasites, time consuming studies involving targetedsampling and probing approaches are still needed. Even thesparse information available on hyperparasites highlights theirpotential in many ecosystem processes. Zoosporic hyperparasitesmay increase the turn-around time of certain nutrients in foodwebs due to their often rapid life cycles. They may play a rolein trophic upgrading, as well as in the stability and complexityof food web dynamics. Hyperparasites also may play a role inthe natural regulation of their host population sizes, which arealso parasites. Regulation of population sizes of parasites willhave an impact on their host population sizes. This may resultin fine-tuning the magnitudes of patterns of energy flow infood webs and impact overall biodiversity as well as populationdynamics. In summary, it is likely that zoosporic hyperparasitesplay a vital part of every ecosystem; hence more focused researchon these important organisms is needed.

AUTHOR CONTRIBUTIONSFrank H. Gleason and Sigrid Neuhauser drafted the initial versionof the manuscript. Agostina V. Marano, Télesphore Sime-Ngando,Martin Kirchmair, Brooke K. Sullivan and Osu Lilje criticallyrevised this draft and contributed intellectual content to the finalversion.

ACKNOWLEDGMENTSSigrid Neuhauser gratefully acknowledges funding by theAustrian Science Fund (FWF) through an Erwin Schrödingerresearch grant (J3175-B20). Frank H. Gleason thanks the

University of Sydney Library for the use of its resources,Elayna Truszewski, Department of Biological Sciences, MacquarieUniversity for her editorial assistance with preparation of thismanuscript.

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Conflict of Interest Statement: The reviewer, Hicham El Alaoui, declares thatdespite being affiliated to the same institution and department as the author,Télesphore Sime-Ndando, the review process was handled objectively and noconflict of interest exists. The authors declare that the research was conducted inthe absence of any commercial or financial relationships that could be construedas a potential conflict of interest.

Received: 14 February 2014; paper pending published: 17 March 2014; accepted: 05May 2014; published online: 28 May 2014.Citation: Gleason FH, Lilje O, Marano AV, Sime-Ngando T, Sullivan BK, Kirchmair Mand Neuhauser S (2014) Ecological functions of zoosporic hyperparasites. Front.Microbiol. 5:244. doi: 10.3389/fmicb.2014.00244This article was submitted to Aquatic Microbiology, a section of the journal Frontiersin Microbiology.Copyright © 2014 Gleason, Lilje, Marano, Sime-Ngando, Sullivan, Kirchmair andNeuhauser. This is an open-access article distributed under the terms of the CreativeCommons Attribution License (CC BY). The use, distribution or reproduction in otherforums is permitted, provided the original author(s) or licensor are credited and thatthe original publication in this journal is cited, in accordance with accepted academicpractice. No use, distribution or reproduction is permitted which does not comply withthese terms.

Frontiers in Microbiology | Aquatic Microbiology May 2014 | Volume 5 | Article 244 | 10